Ancient DNA of the extinct Jamaican monkey Xenothrix reveals extreme insular change within a morphologically conservative radiation

Abstract

The insular Caribbean until recently contained a diverse mammal fauna including four endemic platyrrhine primate species, all of which died out during the Holocene. Previous morphological studies have attempted to establish how these primates are related to fossil and extant platyrrhines, whether they represent ancient or recent colonists, and whether they constitute a monophyletic group. These efforts have generated multiple conflicting hypotheses, from close sister-taxon relationships with several different extant platyrrhines to derivation from a stem platyrrhine lineage outside the extant Neotropical radiation. This diversity of opinion reflects the fact that Caribbean primates were morphologically extremely unusual, displaying numerous autapomorphies and apparently derived conditions present across different platyrrhine clades. Here we report ancient DNA data for an extinct Caribbean primate: a limited-coverage entire mitochondrial genome and seven regions of nuclear genome for the most morphologically derived taxon, the Jamaican monkey Xenothrix mcgregori We demonstrate that Xenothrix is part of the existing platyrrhine radiation rather than a late-surviving stem platyrrhine, despite its unusual adaptations, and falls within the species-rich but morphologically conservative titi monkey clade (Callicebinae) as sister to the newly recognized genus Cheracebus These results are not congruent with previous morphology-based hypotheses and suggest that even morphologically conservative lineages can exhibit phenetic plasticity in novel environments like those found on islands. Xenothrix and Cheracebus diverged ca. 11 Ma, but primates have been present in the Caribbean since 17.5-18.5 Ma, indicating that Caribbean primate diversity was generated by multiple over-water colonizations.

Keywords: Callicebus; biogeography; extinct mammal; island evolution; phylogeny.

Fig. 1.

Upper dentitions of platyrrhine monkeys, comparing (A) the most complete known skull of X. mcgregori, preserving P3-M2 (AMNH 268006), (B) the copper titi monkey, Plecturocebus cupreus (AMNH 34636), and (C) Azara’s night monkey, Aotus azarae (AMNH 94133). (Scale bar: 1 cm.) Important morphological features of Xenothrix: (i) two rather than three molars (differs from all known platyrrhines except non-Callimico callitrichines); (ii) swollen cusps on molars (resembling pitheciids in general, including callicebines); (iii) third premolar is premolariform (specifically resembling callicebines among pitheciids); (iv) incisor alveoli indicate that incisors were probably primitively slender (not expanded as in Aotus).

Fig. 2.

Five alternative tree topologies illustrating previously proposed phylogenetic hypotheses about the evolutionary affinities of Xenothrix. H1: Genus-level tree with Xenothrix as sister to Callicebus within Pitheciidae (23). H2: Genus-level tree with Xenothrix as sister to Aotus within Cebidae (27). H3: Genus-level tree with Xenothrix as sister to Aotus within Pitheciidae (27). H4: Genus-level tree with Xenothrix falling outside all extant platyrrhine families (31). H5: Species-level tree with Xenothrix as sister to all recently recognized callicebid genera (23, 28).

Fig. 3.

Genus-level ML phylogeny generated using whole mitochondrial genomes and produced in RAxML, using data sequenced in this study for Xenothrix and data for 15 other primate genera from GenBank, and with Macaca fuscata selected as the outgroup. Node values represent bootstrap support (100 replicates).

Fig. 4.

Time-calibrated phylogeny showing estimated divergence dates for Xenothrix, 14 other callicebine species, and 5 other platyrrhine genera. Estimates of median divergence dates are shown in red above nodes. Node bars indicate 95% highest posterior density values. Branch values represent posterior probabilities.